Accepted Manuscript

saudimassiliensis” sp. nov. a new bacterial species isolated from air samples in the urban environment of Makkah, Saudi Arabia

Anastasia Papadioti, Esam Ibraheem Azhar, Fehmida Bibi, Asif Jiman-Fatani, Sally M. Aboushoushah, Muhammad Yasir, Didier Raoult, Emmanouil Angelakis

PII: S2052-2975(16)30156-1 DOI: 10.1016/j.nmni.2016.12.019 Reference: NMNI 286

To appear in: New Microbes and New Infections

Received Date: 7 December 2016 Revised Date: 26 December 2016 Accepted Date: 26 December 2016

Please cite this article as: Papadioti A, Azhar EI, Bibi F, Jiman-Fatani A, Aboushoushah SM, Yasir M, Raoult D, Angelakis E, “Arthrobacter saudimassiliensis” sp. nov. a new bacterial species isolated from air samples in the urban environment of Makkah, Saudi Arabia, New Microbes and New Infections (2017), doi: 10.1016/j.nmni.2016.12.019.

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1 “Arthrobacter saudimassiliensis ” sp. nov. a new bacterial species isolated from air

2 samples in the urban environment of Makkah, Saudi Arabia

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4 Running head: “Arthrobacter saudimassiliensis ” sp. nov.

5

6 Anastasia Papadioti 1, Esam Ibraheem Azhar 2,3 , Fehmida Bibi 2, Asif Jiman-Fatani 4, Sally

7 M. Aboushoushah 2, Muhammad Yasir 2, Didier Raoult 1,2 , Emmanouil Angelakis 1*

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9 1 Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes: URMITE

10 CNRS-IRD 198 UMR 6236, Aix Marseille Université, Faculté de Médecine, 27 Bd Jean

11 Moulin, 13385 Marseille, France 12 2Special Infectious Agents Unit, King Fahd MedicalMANUSCRIPT Research Center, King Abdulaziz 13 University, Jeddah, Saudi Arabia

14 3Department of Medical Laboratory Technology, Faculty of Applied Medical Sciences, King

15 Abdulaziz University, Jeddah, Saudi Arabia

16 4Department of Medical Microbiology and Parasitology, Faculty of Medicine, King

17 Abdulaziz University, Jeddah, Saudi Arabia

18 *Corresponding author 19 Phone: (33) 491ACCEPTED 38 55 17, Fax: (33) 491 83 03 90 20 Email: [email protected]

21 Key words: “Arthrobacter saudimassiliensis ” sp. nov. , culturomics, new species, Saudi

22 Arabia, air isolates

ACCEPTED MANUSCRIPT 23 Abstract

24 We report here the main characteristics of ‘ Arthrobacter saudimassiliensis ’ strain

25 11W110_air Τ (CSUR P1223), a new species of the Arthrobacter genus that was isolated from

26 air samples in the city environment of Makkah, Saudi Arabia, during the pilgrim period of

27 Hajj 2012.

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ACCEPTED MANUSCRIPT 45 As a part of a wider culturomics [1] and metagenomics study [2] in Saudi Arabia we

46 isolated a new bacterium named strain 11W110_air Τ from two air samples in the urban

47 environment of Makkah, Saudi Arabia, during the pilgrim period of Hajj 2012. No

48 identification was obtained for the strain 11W110_air Τ using our systematic matrix-assisted

49 laser desorption–ionization time-of-flight mass spectrometry (MALDI-TOF-MS) screening

50 on a MicroFlex spectrometer (Bruker Daltonics, Bremen, Germany) [3]. The strain

51 11W110_air Τ was cultured in 5% sheep blood-enriched Columbia agar (bioMérieux, Marcy

52 l'Étoile, France) for 1 day in an aerobic atmosphere at 37°C. Growth was observed only in

53 aerobic conditions and no growth occurred in anaerobic ones. Colonies on Columbia agar

54 were opaque, round and of yellow color. Optimal growth for this strain was obtained at 37°C

55 at pH 7. The strain 11W110_air Τ is a Gram - positive bacterium, aerobic, motile, catalase

56 positive and oxidase negative.

57 The complete 16S rRNA gene was sequenced using fD1-rP2 primers as previously 58 described and a 3130-XL sequencer (Applied Bioscien MANUSCRIPTces, Saint Aubin, France) [4]. The 59 strain 11W110_air Τ exhibited a 97.4% sequence similarity with Arthrobacter luteolus

60 (NR025362) which was the phylogenetically closest species with standing nomenclature

61 (Figure 1). Consequently, it putatively classifies the strain 11W110_air Τ as a new member of

62 the genus Arthrobacter within the family in the phylum . A.

63 luteolus was first described by Wauters et al . in 2000 as aerobic, gram-positive coryneform

64 isolated from an infected surgical wound [5]. So far, the genus Arthrobacter includes 65 more than 87 speciesACCEPTED with validly published names 66 (http://www.bacterio.cict.fr/c/arthrobacter.html).

67 Strain 11W110_air Τ exhibited a 16S rRNA gene sequence divergence >1.3% with A.

68 luteolus , the closest related species with standing in nomenclature , which classifies it as a

69 new representative of the Arthrobacter genus isolated from air samples in the urban

ACCEPTED MANUSCRIPT 70 environment of Makkah. As a result, we propose the creation of ‘ Arthrobacter

71 saudimassiliensis ’ sp. nov., and the strain 11W110_air Τ as the type strain.

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73 MALDI-TOF-MS spectrum accession number

74 The MALDI-TOF-MS spectrum of “11W110_air Τ” is available at:

75 http://www.mediterranee-infection.com/article.php?laref=256&titre=urms-database.

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77 Nucleotide sequence accession number

78 The 16S rRNA gene sequence of the strain 11W110_airΤ was deposited in GenBank

79 under accession number HG931344.

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81 Deposit in a culture collection

Τ 82 Strain 11W110_air was deposited in the CollectionMANUSCRIPT de Souches de l’Unité des 83 Rickettsies (CSUR, WDCM 875) under number P1223.

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85 Conflict of Interest

86 None

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88 Acknowledgements 89 This workACCEPTED was funded by the Deanship of Scientific Research (DSR), King Abdulaziz 90 University, under grant No. (1-141/1433 HiCi). The authors, therefore, acknowledge technical

91 and financial support of KAU.

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ACCEPTED MANUSCRIPT 94 Figure legend

95 Figure 1. Phylogenetic tree highlighting the position of ‘Arthrobacter saudimassiliensis ’

96 relative to other phylogenetically closest members of the Arthrobacter genus. Numbers at the

97 nodes are percentages of bootstrap values obtained by repeating 500 times the analysis to

98 generate a majority consensus tree. Only values > 95% were displayed. The scale bar

99 represents a 0.5% nucleotide sequence divergence.

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104 105 106 Reference List 107 108 1. Angelakis E, Yasir M, Azhar EI, Papadioti A, Bibi F, Aburizaiza AS, et al . MALDI- 109 TOF mass spectrometry and identification of new bacteria species in air samples 110 from Makkah, Saudi Arabia. BMC ResMANUSCRIPT Notes 2014; 7: 892. 111 2. Angelakis E, Yasir M, Bachar D, Azhar EI, Lagier JC, Bibi F, et al . Gut microbiome 112 and dietary patterns in different Saudi populations and monkeys. Sci Rep 2016; 113 6: 32191.

114 3. Seng P, Drancourt M, Gouriet F, La Scola B, Fournier PE, Rolain JM, et al . Ongoing 115 revolution in bacteriology: routine identification of bacteria by matrix-assisted 116 laser desorption ionization time-of-flight mass spectrometry. Clin Infect Dis 117 2009; 49: 543-551.

118 4. Safont M, Angelakis E, Richet H, Lepidi H, Fournier PE, Drancourt M, et al . Bacterial 119 lymphadenitis at a major referral hospital in France from 2008 to 2012. J Clin 120 Microbiol 2014; 52: 1161-1167.

121 5. Wauters G, Charlier J, Janssens M, Delmee M. Identification of Arthrobacter oxydans , 122 ArthrobacterACCEPTED luteolus sp. nov., and Arthrobacter albus sp. nov., isolated from 123 human clinical specimens. J Clin Microbiol 2000; 38: 2412-2415. 124 125 ACCEPTED MANUSCRIPT

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